Association of Inflammatory Periapical Lesions with Maxillary Sinus Abnormalities: a Retrospective Cone-Beam Computed Tomography Study

Statement of the Problem: Odontogenic infections such as periapical lesions (PLs) can cause changes in the adjacent tissues. Infection of the maxillary posterior teeth can be easily transmitted to the maxillary sinus and cause changes in the maxillary sinus mucosa. Cone-beam computed tomography (CBCT) has high accuracy and sensitivity for detection of odontogenic lesions and is efficient for maxillary sinus assessment. Purpose: This study aimed to assess the maxillary sinuses for abnormalities such as mucosal thickening, polyps, and periostitis, and evaluate the periapical status of maxillary posterior teeth considering the presence of PLs, their size and distance from the sinus floor by evaluating CBCT images. Materials and Method: This retrospective, cross-sectional study evaluated the CBCT scans of 143 patients, depicting the posterior maxilla with at least one premolar or molar tooth present in this region. Sinus abnormalities (mucosal thickening, sinus polyps, and periostitis) and presence/ absence of PLs, its size, and its distance from the sinus floor were all assessed on CBCT scans. Data were analyzed using the Chi-square test in SPSS version 21 (a= 0.05). Results: PLs were observed in 31.2% of the cases. In presence of PLs, mucosal thickening was noted in 56.8%, sinus polyps in 29.6% and periostitis in 1.3% of the maxillary sinuses. All teeth with a CBCT periapical index (CBCTPAI) score of 5 were associated with sinus abnormalities; there was neither correlation between the sizes of lesions, nor their distance from the sinus floor with sinus abnormalities (p> 0.05). Conclusion: PLs in the posterior maxilla have a direct correlation with the maxillary sinus abnormalities. However, the size or distance of PLs from the sinus floor had no significant effect on the frequency of sinus abnormalities.


Introduction
Following dental pulp necrosis, infection may spread into the periapical space and cause pathological changes in the periapical tissues. The interactions between the stimulants leaked out from the canal space and the host response can lead to activation of host immunity reactions. The infection at the periapical region of the maxillary posterior teeth can extend to the maxillary sinus via the blood and lymphatic vessels and cause sinus diseases [1], which may vary from a simple sinusitis to severe rhino sinusitis and even brain abscess, depending on the severity of tooth infection [2].
The maxillary sinusitis (MS) is a common condition with significant health-related complications [3]. Traditionally, odontogenic MS has been stated to account for 10%-12% of all cases of MS, an analysis of recent data indicates a much higher prevalence of 30%-40% [4]; 83 percent of these are reportedly due to apical and marginal periodontitis [5]. Recent studies have documented correlations between dental pathology and radiographic signs of sinusitis, predominantly mucosal thickening of the Schneider membrane [6][7][8][9].
Identifying the relationship between odontogenic and sinusal pathologies is essential to establish the correct diagnosis and management of the patient [10]. In the otolaryngology literature, odontogenic MS is reported to be underdiagnosed and often overlooked, leading to persistent symptoms in patients and the failure of medical and surgical sinusitis therapy [4,11].
Radiographs are effective instruments in diagnosis of periapical changes and MS abnormalities [12]. Radiographs, however, are 2-dimensional (2D) representations of 3-dimensional (3D) structures, making it particularly difficult to determine the relationship of roots and periapical lesions (PLs) with the MS floor [13,5]. Conebeam computed tomographic (CBCT) imaging is capable of producing high-quality 3-dimensional images using a reduced dose of radiation and has a lower cost compared to multi-slice computed tomographic imaging [14].CBCT imagery enables the detection of changes in the maxillary sinus and their possible causes [7]. This is an ideal examination tool for assessing patients who have both dental and sinus complaints [15], and is considered as a useful technique to evaluate the relationship between maxillary sinus and adjacent teeth [4]. This retrospective, cross-sectional study aimed to assess the maxillary sinuses for abnormalities such as mucosal thickening, polyps and periostitis, and to evaluate the periapical status of maxillary posterior teeth in terms of presence of PLs, their size and distance from the sinus floor by evaluating CBCT images obtained from an archived collection. CBCT scans that requested because of trauma or developmental anomalies or showed an orthodontic retainer, skeletal deformities, suspected cases of tumors in the maxillary sinus, pansinusitis and history of previous surgery and related dental procedures were excluded. In addition in case of possibility of any errors in measurements when assessing the sinus and PLs, the sample would be excluded right away.

Maxillary sinus assessments
The findings obtained by evaluation of the maxillary sinus images were classified as follows ( Figure 1) [12,16].

Normal
The sinus space was completely radiolucent, the cortical walls were sound and intact, and there was no mucosal thickening.

Mucosal thickening
In some areas, the cortical bone was lost and the soft tissue density could be observed. Mucosal thickening was

Sinus polyps
Some polypoid and lobulated areas with observable soft tissue density without cortical bone were noted while the sinus floor was sound and intact.

Periostitis
Uniform opaque areas of layered thickening in the cortical bone of the sinus floor were noted superior to a radiolucent area related to tooth apex.
The CBCT images were evaluated three-dimensionally, and four measurements were made including sagittal (mesiodistal), coronal (buccolingual), and axial (mesiodistal and buccolingual). The maximum extension of lesion was recorded as the reference size and scored using a 6-point scoring system (0-5) as follows ( Figure 2) [17].

Assessment of periapical status
The teeth with a hypo dense PLs were recorded. The In teeth with multiple PLs, the lesion with the most severe pathological condition was recorded.
The lesions were divided into three groups based on their distance from the sinus floor as 0 mm (the lesion was attached to the maxillary sinus floor), 0-2 mm distance and > 2 mm distance.
Moreover, the maxillary sinuses were divided into two groups based on presence/absence of PLs in the posterior maxilla as (1) with at least one PL in teeth adjacent to the sinus, and (2) no tooth with PL. All images were observed by an oral and maxillofacial radiologist. In order to assess the intraobserver agreement, first 20% of the primary sample (56 images) was observed by the observer twice with a three months interval.

Statistical analysis
Data were analyzed using SPSS version 21 (SPSS Inc., IL, USA). The prevalence of sinus pathologies was calculated in presence/absence of PLs. The results were analyzed using the Chi-square test and the correlation coefficients. The intraobserver agreement was evaluated using the kappa coefficient, and the level of significance was set at α=0.05.

Results
The kappa coefficient of intra-observer agreement was   The use of CBCT imaging in dentistry has made 3D studies of maxillofacial structures possible and has contributed significantly to the identification of PLs and the evaluation of their impact on complex clinical condition [20][21][22][23]. CBCT imaging is considerably more sensitive than conventional radiographs and is extremely useful in investigating the involvement of MS associated with periapical infections [7,13,5,22].
Nascimento et al. [10] evaluated the integrity of the maxillary sinuses adjacent to PLs and reported the accuracy, sensitivity and specificity of CBCT images to be low, good and variable, respectively; low accuracy of CBCT in their study was attributed to the low interobserver agreement and noisy images. The main limitations of CBCT include higher scatter radiation compared with medical CT as well as metal artifacts, commonly caused by metals and amalgam restorations and less commonly caused by root filling materials and dental implants [23]. In this study, images with artifacts were excluded.
At present, the CBCT systems can be divided into two groups of small (dental and regional) or large (ortho or facial) scale based on the size of FOV. The voxel size in systems with a small FOV is small (0.2-0.1 mm); thus, such systems have higher resolution and are more suitable for endodontic applications [24]. Therefore, in this study, a CBCT system with a small FOV was used to better visualize the anatomical structures in greater details. Shanbhag et al. [5] showed that CBCT is an efficient imaging modality for detection of periapical disease and sinus mucosal thickening; this statement has also been confirmed by some other studies [10,[25][26][27][28], as well as the current study.
Mucosal thickening is an inflammatory reaction characterized by the hyperplasia of the maxillary sinus mucosal epithelial cells [29]. In general, mucosal thickening is the most common maxillary sinus abnormality with a prevalence rate of 37% to 62% [8]. Controversy in the reported prevalence rates can be due to two reasons including different diagnostic criteria employed by different studies, and no consensus reached on minimal mucosal thickness to be considered normal; the minimal pathological thickness is believed to be 1-3 mm.
According to Inusua et al. [25], sinus mucosal thickening on CBCT scans is greater than that detected by histological analysis. Thus, thicknesses > 1 mm are considered as pathological mucosal thickening on CBCT scans. In our study, thicknesses > 1 mm were considered as mucosal thickening and accordingly, the frequency of mucosal thickening in our study population was found to be 35%; such a low rate was due to the set inclusion criteria, since we tried to eliminate abnormalities with non-odontogenic origin.
The current results revealed pathological changes in 87.7% of the maxillary sinuses in presence of PLs in the posterior maxilla, which was in agreement with the results of Shanbhag et al. [5] and Lu et al. [9]. However, Nunes et al. [12]  This process decreases the observer errors in measurements compared with 2D radiography [17]. In this study, the CBCTPAI was used considering the high accuracy of CBCT for this purpose. Nunes et al. [12] also used CBCTPAI and found no significant correlation between the size of lesions and sinus abnormalities.
In our study, the size of lesions had no significant correlation with the maxillary sinus abnormalities. Nonetheless, it may be stated that presence of PLs > 8 mm would be associated with sinus abnormalities. Lu et al. [9] used periapical index in their study and reported sinus abnormalities in all patients with acute PLs; however, they did not find a significant association between the size of lesions and sinus abnormalities. Thus, both of the abovementioned studies support our findings.
Approximation of the PL to the maxillary sinus floor may be a potential factor stimulating the sinus mucosa.
In this study, the effect of distance between the upper limit of the PL and the maxillary sinus floor on sinus abnormalities was also analyzed. The Chi-square test revealed no significant correlation between the maxillary sinus abnormalities and the distance between the PL and the sinus floor. Lu et al. [9] and Rege et al. [31] discussed that the position of PL relative to the maxillary sinus had no significant effect on mucosal thickening. In contrast to our findings, Nunes et al. [32] discussed that maximum sinus abnormalities were noted when the distance between the PL and the maxillary sinus floor was 0 mm. In general, it may be stated that

Conclusion
Within the limitations of this study, maxillary posterior teeth association periapical radiolucent lesions had the highest frequency of sinus abnormalities. The size of a PL and close spatial relationship between the PL and the sinus was not associated with the frequency of sinus abnormalities. Accidental maxillary sinus findings on CBCT scans warrant thorough differential diagnosis.
Frequently, they may be related to dental pathologies.